Jeffrey C. Carrier

Biology of sharks and their relatives

Phylogeny and Zoogeography The Origin and Relationships of Early Chondrichthyans Eileen D. Grogan, Richard Lund, and Emily Greenfest-Allen Elasmobranch Phylogeny: A Mitochondrial Estimate Based on 595 Species Gavin J.P. Naylor, Janine N. Caira, Kirsten Jensen, Kerri A.M. Rosana, Nicolas Straube, and Clemens Lakner Phylogeny of Batoidea Neil C. Aschliman, Kerin M. Claeson, and John D. McEachran Phylogeny, Biology, and Classification of Extant Holocephalans Dominique A. Didier, Jenny M. Kemper, and David A. Ebert Form, Function, and Physiological Processes Biomechanics of Locomotion in Sharks, Rays, and Chimeras Anabela M.R. Maia, Cheryl A.D. Wilga, and George V. Lauder Prey Capture Behavior and Feeding Mechanics of Elasmobranchs Philip J. Motta and Daniel R. Huber Energetics, Metabolism, and Endothermy in Sharks and Rays Diego Bernal, John K. Carlson, Kenneth J. Goldman, and Christopher G. Lowe Food Consumption and Feeding Habits Bradley M. Wetherbee, Enric Cortes, and Joseph J. Bizzarro Integrative Multisensor Tagging: Emerging Techniques to Link Elasmobranch Behavior, Physiology, and Ecology Nicholas M. Whitney, Yannis P. Papastamatiou, Adrian C. Gleiss Reproductive Biology of Elasmobranchs Christina L. Conrath and John A. Musick Hormonal Regulation of Elasmobranch Physiology James Gelsleichter and Andrew N. Evans Sensory Physiology and Behavior of Elasmobranchs Jayne M. Gardiner, Robert E. Hueter, Karen P. Maruska, Joseph A. Sisneros, Brandon M. Casper, David A. Mann, Leo S. Demski Recent Advances in Elasmobranch Immunology Carl A. Luer, Catherine J. Walsh, and Ashby B. Bodine Ecology and Life History Assessing the Age and Growth of Chondrichthyan Fishes Kenneth J. Goldman, Gregor M. Cailliet, Allen H. Andrews, and Lisa J. Natanson Population Dynamics, Demography, and Stock Assessment Enric Cortes, Elizabeth N. Brooks, and Todd Gedamke Genetics of Sharks, Skates, and Rays Edward J. Heist Predator-Prey Interactions Michael R. Heithaus and Jeremy J. Vaudo An Updated Look at Elasmobranchs as Hosts of Metazoan Parasites Janine N. Caira, Claire J. Healy, and Kirsten Jensen Assessing Habitat Use and Movement Colin A. Simpfendorfer and Michelle R. Heupel Index

A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum

Elasmobranch reproductive behavior has been inferred from freshly caught specimens, laboratory examinations of reproductive structures and function, or determined from direct observations of captive or free swimming wild animals. Several general behaviors have been described including seasonal sexual segregation, courtship and copulation. Courtship behavior was inferred for many species from the presence of scars and tooth cuts on the females body, and noted in more detail from underwater observations. Copulation has been directly observed in captive settings for several species of elasmobranchs in large aquaria, and in the wild for three species of urolophids and for Triaenodon obesus and Ginglymostoma cirratum. A detailed ‘case history’ of nurse shark reproductive behavior is presented that may be used as a template for future work on shark reproductive behavior of other species. Our studies, using diver identifiable tags and in situ behavioral observations, provide unprecedented information on social structure and mating behavior in this species. Since 1993, 115 G. cirratum, 45 adults and 70 juveniles have been tagged in the Dry Tortugas, Florida. Observations show that adult males visit the study site every year with three males dominant. Individual adult females visit the study area to mate in alternate years. Polygyny and polyandry are common. Future research on reproductive behavior of elasmobranchs should address questions on male access to females, sexual selection and dominance hierarchies.

Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum

Fifty mating events in free-living nurse sharks (Ginglymostoma cirratum) were observed over a nine-day period in the Dry Tortugas island cluster in the Florida Keys. Four stages of mating were identified: precoupling, coupling, positioning and alignment, and insertion and copulation. Copulation was observed and filmed in four of the mating events. Seminal fluid released into the water was obtained following one copulation and showed the presence of free, nonpackaged sperm cells. At least 10 of the events involved multiple males attempting copulation with single females.

Sharks and their relatives II : biodiversity, adaptive physiology, and conservation

CHONDRICHTHYAN BIODIVERSITY: ECOSYSTEMS AND DISTRIBUTION OF FAUNA Epipelagic Oceanic Elasmobranchs John D. Stevens Deepwater Chondrichthyans Peter M. Kyne and Colin A. Simpfendorfer Chondrichthyans of High Latitude Seas David A. Ebert and Megan V. Winton Elasmobranchs of Tropical Marine Ecosystems William T. White and Emma Sommerville Biology of the South American Potamotrygonid Stingrays Ricardo S. Rosa, Patricia Charvet-Almeida, and Carla Christie Diban Quijada Life History Strategies of Batoids Michael G. Frisk ADAPTIVE PHYSIOLOGY Ontogenetic Shifts in Movements and Habitat Use R. Dean Grubbs Tracking and Analysis Techniques for Understanding Free-Ranging Shark Movements and Behavior David W. Sims Sensory Adaptations to the Environment: Electroreceptors as a Case Study Stephen M. Kajiura, Anthony D. Cornett, and Kara E. Yopak Molecular Insights into Elasmobranch Reproductive Behavior for Conservation and Management David S. Portnoy Physiological Responses to Stress in Sharks Gregory Skomal and Diego Bernal Pollutant Exposure and Effects in Sharks and Their Relatives James Gelsleichter and Christina J. Walker CONSERVATION Factors Contributing to Shark Attacks on Humans: A Volusia County, Florida, Case Study George H. Burgess, Robert H. Buch, Felipe Carvalho, Brittany A. Garner, and Christina J. Walker Shark Control: Methods, Efficacy, and Ecological Impact Sheldon F.J. Dudley and Geremy Cliff DNA Forensic Applications in Shark Management and Conservation Mahmood S. Shivji Unraveling the Ecological Importance of Elasmobranchs Michael R. Heithaus, Alejandro Frid, Jeremy J. Vaudo, Boris Worm, and Aaron J. Wirsing Life Histories, Population Dynamics, and Extinction Risks in Chondrichthyans Nicholas K. Dulvy and Robyn E. Forrest

Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus

We analysed video records of three mating events involving nine free-living whitetip reef sharks in Cocos Islands, Costa Rica to examine reproductive behaviour in this species. We describe several behaviours never before documented in this species, and four behaviours never before documented in any elasmobranch. Here, we also present the first hypothesis for the function of the males paired reproductive organs, the siphon sacs, to be based on observations of mating sharks. We introduce terminology for three separate siphon sac structural components that are externally visible during courtship and mating in this species. Based on our analyses, as well as evidence from past mating studies, the siphon sacs in whitetip reef sharks appear to be used to propel sperm into the females reproductive tract, not for flushing the females reproductive tract of sperm from previous males. We discuss the implications of ‘group courtship’, ‘siphon isthmus constriction’, ‘reverse thrusting’, ‘postrelease gaping’ and ‘noncopulatory ejaculation’.

Multiple paternity in the nurse shark, Ginglymostoma cirratum

For over a decade, we have been studying the reproductive behavior of the nurse shark, Ginglymostoma cirratum, in the Dry Torugas off the Florida Keys, an important mating and nursery ground for this species. In the course of these studies, we have used a variety of tags and tagging protocols to monitor individual animals. Here we report the use of molecular methods for the genetic analysis of nurse sharks. Specifically we have analyzed genetic variation at the MHC II alpha locus using the polymerase chain reaction (PCR) followed by restriction fragment length polymorphism (RFLP) analysis of the amplified products. We found this technique to be a relatively rapid and reliable method for identifying genetic differences between individual sharks. Applying this method to a family of sharks consisting of a mother and 32 pups, we demonstrate that at least four fathers must have fathered this brood. Multiple paternity in the nurse shark suggests a mechanism by which populations of this species may maximize genetic variability. This seems especially valuable for philopatric species whose migratory movement, and thus potential for genetic diversity, is limited.

Habitat management and closure of a nurse shark breeding and nursery ground

Abstract The nurse shark ( Ginglymostoma cirratum ) is a common resident of Florida and Caribbean waters. In spite of its prevalence, details of nurse shark life history and ecology are not well known. Ongoing studies have identified a population that undergoes mating and parturition in one specific site in the Florida Keys. Our tagging, observation, and filming have demonstrated that reproductive activities occur preferentially for some animals in very shallow coastal waters, and one such site became the study area. From our continuing investigations we have learned that mating activities of the sharks in this area are vulnerable to the disruptive effects of wading, diving, photography (electronic flash), boat traffic, and human presence during the times when mating occurs. To reduce disruptive activities during the mating season, a proposal to protect this mating and nursery grounds was submitted to the National Park Service. Three elements of protection that we felt were critical to implement were to: (1) recognize a specific area as unique and critical to the breeding success of the sharks, (2) restrict the public during times identified by our research as essential for mating, and (3) implement a program of public education.

Exact Enumeration of Sires in the Polyandrous Nurse Shark (Ginglymostoma cirratum)

Abstract Polyandry has been demonstrated in a number of shark species. Studies based on a small number of loci typically estimate the minimum number of sires, which may be much lower than the actual number of sires due to the sharing of alleles by parents. We genotyped three litters of Nurse Shark (Ginglymostoma cirratum) ranging in size from 29 to 39 pups at 12 DNA microsatellite loci to determine the number of sires for each litter. We analyzed the genotypes using two analytical methods, both of which indicated that each litter had five to seven sires with one to 17 pups per sire. Previous analyses of these litters based on MHC loci indicated a minimum of four sires. Because G. cirratum are not capable of long-term sperm storage and ovulate over several weeks, they may require multiple inseminations to fertilize an entire litter. The varying levels of developmental stage among embryos found within a single litter may reflect multiple fertilizations over a prolonged period. Exact enumeration of sires as demonstrated here can provide valuable information for understanding reproductive ecology of live-bearing vertebrates.